Journal of Asia-Pacific Biodiversity 11 (2018) 25e31

Contents lists available at ScienceDirect

Journal of Asia-Pacific Biodiversity

journal homepage: http://www.elsevier.com/locate/japb

Original Article Foraging areas of streaked leucomelas nesting on the Karamzin Island (Peter the Great Bay, East Sea)

Ivan Tiunov a,*, Igor Katin b, Hansoo Lee c, Siwan Lee c, Eunhong Im c a Federal Scientific Center of the East Asia Terrestrial Biodiversity FEB RAS, Laboratory of Ornithology, Vladivostok, Russia b National Scientific Center of Marine Biology FEB RAS, Laboratory of Marine Mammals, Vladivostok, Russia c Korea Institute of Environmental Ecology, Daejeon, The Republic of Korea article info abstract

Article history: Karamzin Island (the Peter the Great Bay, the East Sea) is the only nesting point of streaked Received 25 May 2017 in Russian Federation. To understand and determine distribution patterns of streaked shearwaters along Received in revised form the Eastern Sea waters during nesting period, the Trackers WT-300 were set to 10 adult . Over the 18 September 2017 observation period (from 5 July 2016 to 7 January 2017), 4812 locations were registered. Analysis of data Accepted 17 October 2017 obtained revealed that main feeding points of colony studied were situated in the Peter the Great Bay Available online 21 November 2017 along 50 m isobath and, to the less extension, near the eastern coast of Korean Peninsula. It was determined that streaked shearwaters most frequently visited waters with circular flows or zones of Keywords: fl Foraging area junctions of multidirectional ow. It was also shown that these zones had high concentrations of Streaked shearwater zooplankton. The East Sea Ó 2017 National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA), Publishing The Peter the Great Bay Services by Elsevier. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/).

Streaked shearwater is a numerous subtropical that birds with food may indicate the possibility of sufficient food breeds exclusively in Northwestern part of the Pacific Ocean. In supply not too far from the colony, and border of expansion is Russia, the only breeding colony of this species is situated on the identified as, in most species of petrels, with radius of 200 miles Karamzin Island (the Peter the Great Bay). Population of this colony (Litvinenko 1976). According to the studies performed in the last numbers 80e150 pairs (Shuntov 1998; Litvinenko et al 2000). The half years of 20th century, the Northwestern part of the East Sea’s species is included in the Red book of the Russian Federation and is feeding conditions favorable for birds appear in the summer, and under state protection (Red book of the Russian Federation, 2001). particular great mass of zooplankton accumulates in June that Study of streaked shearwater began in 1959 by Yoshida (Yoshida consequently attracts and different pelagic fish 1962). At the same time, ringing of nestlings and adults was orga- (Meshcheryakova 1960; Shuntov 1965). nized in Japan (McClure 1969). Beside Japan (Yoshida 1981), further Data on streaked shearwater distribution in the East Sea in investigations of streaked shearwater biology was carried out in the summer are limited to ship observation by Shuntov (1998) and Republic of Korea (Lee & Yoo 2002, 2004; Nam et al 2014). From reduced to registration of significant number of adult and imma- 2006 to 2008, the use of geolocators allowed to determine foraging ture birds without specification of meeting areas and connection to areas of birds nesting at Sangan and Mikura Islands, located near specific colonies. the Honshu Island (Yamamoto et al 2011). Karamzin Island is situated in the well-developed area of the In Russia, a study of breeding biology of streaked shearwater Russian Far East, and for this reason experiencing significant using ordinary metallic rings was conducted by Litvinenko anthropogenic pressure. Because of low number of breeding birds (Litvinenko 1976) in 1967e1970. It shows that frequent arrival of as well as the proximity to large center Vladivostok city and the industrial districts of Primorsky region with high population den- sity, the danger that any accident can cause the death of the colony and the disappearance of the species in Russia is exist. Knowledge * Corresponding author. E-mail address: [email protected] (I. Tiunov). about the biology of this species in conditions of the Russian Far Peer review under responsibility of National Science Museum of Korea (NSMK) and East including peculiarities and patterns of spatial distributions of Korea National Arboretum (KNA). streaked shearwaters in the Eastern Sea during nesting period is https://doi.org/10.1016/j.japb.2017.10.005 pISSN2287-884X eISSN2287-9544/Ó 2017 National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA), Publishing Services by Elsevier. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 26 I Tiunov et al. / Journal of Asia-Pacific Biodiversity 11 (2018) 25e31 essential to prevent negative consequences, minimize possible January 2017, when the last tracker had stopped the information damage, and work out the most efficient measures for protection of translation. this unique Russian colony. Clarification of these issues was the main goal of this work. Results

Materials and methods Data from one of the birds (Tracker N 1610) were obtained only once on the next day after Tracer installation. The information flow Karamzin Island is a part of the south archipelago of the Peter from the other (N 1609) stopped on August 3, when the bird the Great Bay (N 42 50 32 E 131 41 20). Approximate area of the was in the eastern part of the bay. Most of the time, the bird spent in island is 0.09 km2 and the highest point is 107 m. A few colonies of the frames of the Peter the Great Bay with the exception of July 20e marine birds (total amount not less than 10,000 pairs) inhabit the 22, when it was registered in the Eastern Sea at the latitude of island. Chongjin and Gilju cities of the Democratic People's Republic of An international agreement between the Institute of Biology Korea. and Soil science FEB RAS (2017dFederal Scientific Center of the Four streaked shearwaters (N 1602, 1605, 1607, and 1608) stayed East Asia Terrestrial Biodiversity) and the Korea Institute of Envi- near the colony till the end of the second decade of July and left the ronmental Ecology (KoEco) was signed in 2016. In the frames of this nesting region after that. It was registered that birds moved along agreement, studies on the character of space use during nesting the Korean Peninsula and spent most of the time in the frames of time of streaked shearwater with the aid of Trackers WT-300 triangle Pohang city e Ulleung Island e Sokcho city. Numbers 1605, (KoEco (Korea Institute of Environmental Ecology), Republic of 1607, and 1608 returned back to the Peter the Great Bay on August Korea) were carried out. 4, 10, and 5, respectively. Tracker N 1605 ceased to send signal, and Ten adults of streaked shearwater were captured in the further location of this bird is unknown. Streaked shearwaters N nesting colony at Karamzin Island on 5 July 2016. Trackers WT- 1607 and 1608 fed in the Peter the Great Bay till the August 28 and 300 (NN 1601e1610) were attached to the bird backs. After that 25 correspondingly. Then, birds moved to the Korean Peninsula, birds were returned to nests. Gender of birds was not identified. where signal from 1608 Tracker was lost near the Uljin city on All sensors were adjusted to define the coordination every 4 September 13 and signal from 1607 was lost in the area of Korea hours. Strait on September 14. In contrast to the latter three birds, streaked Trackers WT-300da telemetry device, which is based on the shearwater N 1602 headed to the South, to Korean Strait, and GPS (Global Positioning System) combined with WCDMA (Wide- further to the Yellow Sea, and fed there till September 12. After it band Code Division Multiple Access) mobile phone network with moved southward and reached the South China Sea. The last signal global roaming system (http://www.wi-tracker.com). Data on 4812 from that bird was received from the waters located south of the locations were obtained over the study period from 5 July 2016 to 7 Chang Jiang river mouth on September 16.

Figure 1. Map of feeding sites of the streaked shearwater N 1604 (white dots) and N 1601 (red dots) in July. I Tiunov et al. / Journal of Asia-Pacific Biodiversity 11 (2018) 25e31 27

Figure 2. Map of feeding sites of the streaked shearwater N 1604 (white dots) and N 1601 (red dots) in August.

Streaked shearwater N 1603 fed exclusively in the Peter the sites of the streaked shearwater N 1601 were situated in the con- Great Bay till the August 25. The bird was registered in the colony tinental terrace to the south up to the Korean Plateau at a distance on August 21 for the last time; after that the bird held on the waters of 400 km from colony (Figure 1). of the bay for a few days, and then moved to the Korean Peninsula In August, the streaked shearwater N 1604 adhered to the same along the coast. It fed near the eastern coast of Korean Peninsula strategy feeding close to the colony in the frames of the Peter the between Sokcho and Pohang cities till the middle of October. After Great Bay, mostly in the waters of the Ussuri Bay at a distance of 5e October 20, the bird crossed Korean Strait and headed to the central 83 km from colony. During that period, it visited the colony every parts of the East China Sea. The last signal from this bird was night with the exception of August 1e2, 22e23, and 27e28, when it received from the waters located south of the Chang Jiang river continuously fed. In August 13e15, the shortest fly distances from mouth on November 8. colony were registered. Moreover, these days it visited the colony The main feeding sites of the streaked shearwater N 1606 sit- during day light. This may indicate that hatching of nestling took uated along continental terrace to the south up to Ulleung Island, place these days. The streaked shearwater N 1601 spent 2e3 days at where it spent 36 days in total. In the Peter the Great Bay, the bird the nest and preferred to move in the food searching at large dis- fed rare and spent here 21 days in total. The maximum period of tances (up to 520 km from colony) and fed on the waters at sea- incubating laying was 8 days (July 15e23). The streaked shearwater mounts Ostrovnaya, Sibir, Koltso, and at the continental terrace to fed near the colony from August 17e19, and came back to the nest the south up to Korean Plateau (Figure 2). at night. It may indicate that a nestling has hatched at that time. The main feeding sites of two birds situated in the waters of the After another night at the colony, the bird headed to the south to Peter the Great Bay in September. At the same time, both birds took the Korean Peninsula on September 20, thus leaving the nesting flights far to the south up to Korean Plateau in search of food area. (Figure 3). Two streaked shearwaters (N 1601 and 1604) stayed near the colony the longest. They migrated to the south on October 3 and 5, Discussion respectively. During July, the main feeding spots of the streaked shearwater N Based on the analyses of spatiotemporal scheme of birds mov- 1604 were situated in the waters of the Peter the Great Bay and its ing, it may be assumed that nest of the streaked shearwaters vicinity at a distance of 60 km from colony. Periods of continuous N 1602, 1605, 1607, and 1608 were destroyed at the laying stage, incubation were 9, 4, and 3 days (July 7e15, July 21e25, and July whereas the birds N 1603 and 1606 lost their nestlings. Nesting 27e29, respectively). In contrast with this bird, the main feeding season was successful for birds N 1601 and 1604 because they most 28 I Tiunov et al. / Journal of Asia-Pacific Biodiversity 11 (2018) 25e31

Figure 3. Map of feeding sites of the streaked shearwater N 1604 (white dots) and N 1601 (red dots) in September. probably left colony after fledging. This is in agreement with almost naked. Such places are ease to access, but they are more Litvinenko’s data (1976). According to her, young birds leave the often exposed to destruction by predators, the role of which is colony in the period between the third decade of October and the played by Slaty-backed Gull, Black-tailed Gull, and Large-billed first decade of November. Nestlings stay in the nest 10e19 days Crow. Considering these circumstances and also the high death after the last feeding. rate (up to 54%) at the island (Litvinenko 1976), data obtained were Loss of laying and nestlings from marked birds is connected quite expectable. with relative availability of nests. Thus, some specimens were Data about the feeding time of adult birds, brooding frequency, found in nests situated in small niches under stones and were and the duration of the lack of feeding birds greatly expand the

800

700

600

500

400 km

300

200

100

0

. . . . 7. 7 7. 7 8 8. 9. .09. .0 3.08. 5.08. 9.08. 1.08. 4 6.09. 0 8.09. 2.10. 06.0 10.0 14.07. 18.0 22.0 26.07. 30.07. 0 07.0 11.08. 1 1 23.08. 27.0 3 0 08.09. 12.09 1 2 24.09. 2 0

Figure 4. The average distance of feeding expansion of three streaked shearwaters. Dashed linedN 1604, solid linedN 1601, and gray linedN 1606. I Tiunov et al. / Journal of Asia-Pacific Biodiversity 11 (2018) 25e31 29

Figure 5. Feeding sites of streaked shearwaters from the Karamzin Island colony.

Figure 6. Main foraging areas of the streaked shearwaters from the Karamzin Island colony in the Peter the Great Bay. available information (Litvinenko 1976). Author indicates that one Significant difference in behavior, flying distance, and feeding of the partners may spend a few days (up to 8 days) out of nest time on the example of three birds (Figure 4) may be explained by while the other one ever-present brood nests. According to our both differences in the gender as well as personal peculiarities. data, birds can spend up to 12 days out of colony (6e8 days usually) According to existing data (Yamamoto et al 2011), there are slight while the maximum of ever-present brooding time was 9 days. differences in flying distances and duration of feeding time 30 I Tiunov et al. / Journal of Asia-Pacific Biodiversity 11 (2018) 25e31

Figure 7. Map of regular surface currents in the Peter the Great Bay and adjacent waters of the Eastern Sea (Sailing direction 1996). Red line indicates main feeding area of streaked shearwaters. between birds, but these differences were registered only during Japanese colleges (Yamamoto et al 2011) that studied feeding the preparation of egg laying in April and May. During the incu- sites of streaked shearwaters from the Honshu Island colonies us- bation period, this difference was not such obvious. ing geolocators have found the correlations between the region of Data analyses show that the main feeding area of streaked feeding and zooplankton concentration. The latter attract different shearwaters during nesting period was situated in the Peter the species of pelagic fish that are the main food source for streaked Great Bay and to the less extension in the region of continental shearwaters. It was also shown that the main feeding sites were terrace of Korean Plateau waters (Figure 5). The most visited situated at a distance of 240e500 km from the colony, and the feeding spots in the Peter the Great Bay are situated in region with maximum expansion of birds in food search can reach 800 km 50-meter depth and the South in the direction of increasing depth (Yamamoto et al 2011). (Figure 6). A comparison of the main feeding spots of streaked During nesting period, the main feeding areas of streaked shearwaters with the scheme of surface currents (Figure 7) shows shearwaters from Karamzin Island are located at a distance of 1e that they are well superimposed on the zones of circular currents 80 km from the colony and connected with the neritic zones with and places where multidirectional currents converge. It is neces- about 50-m depth. These zones are characterized with the most sary to mention that circular currents and multidirectional currents density of zooplankton (Figure 8)(Dolganova and Nadtochii 2015). are situated near the Korean Peninsula (Leonov 1960), where Beside these waters, the streaked shearwaters from Karamzin Is- streaked shearwaters fed as well. land colony were regularly flying to the Korean Peninsula up to

Figure 8. Map of distribution of zooplankton biomass in the Peter the Great Bay in summer (Dolganova and Nadtochii 2015). Red line indicates main feeding area of streaked shearwaters. I Tiunov et al. / Journal of Asia-Pacific Biodiversity 11 (2018) 25e31 31

36 km parallel (N 36 32), i.e., 720 km from the colony. In addition, Lee KG, Yoo JC. 2002. Breeding population of Streaked Shearwaters and the effect of e the birds were flying to the Eastern Sea at a distance up to 250 km Norway predation on Sasudo Island. J. Yamashina Inst. Orn 33:142 147. Lee KG, Yoo JC. 2004. Variation in chick provisioning of Streaked Shearwaters reaching underwater mountains Koltso, Sibir, and Ostrovnaya (Calonectris leucomelas) during the early nestling stage. Journal of the Yamashina (Figure 5). Institute Ornithology 35:105e119. Leonov AK. 1960. The Sea of Japan. Regionalnaya okeanografiya. Gidrometeoisdat. pp. 291e463 (in Russian). Conclusions Litvinenko NM. 1976. Breeding biology of Streaked Shearwater (Puffinus leucome- las). Zoolgicheskii Zhurnal 55:1206e1213 (in Russian). The border of feeding area of the northwest colony of streaked Litvinenko NM, Zhirmunsky AV, Tkachenko KS. 2000. To including small islands in fi the Peter the Great Bay into Far Eastern marine reserve. Vestnik DVO RAN V 1: shearwater was de ned solely through the use of Trackers WT-300. 50e56 (in Russian). It was also shown that in the food search, birds may reach the McClure HE. 1969. Migratory pathological survey, Ann. progress report 1968. southern part of the Korean Peninsula. Although the main feeding Far East: U.S. Army research and development group. pp. 1e340. Meshcheryakova IM. 1960. Seasonal changes of plankton in the open waters of the areas are situated in the immediate vicinity of the colony at the Sea of Japan. Izvestiya Tikhookeanskogo Instituta Morskogo I Ribnogo Khozaystva I distance 1e80 km, it is revealed that the most visited feeding spots Okeanografii 46:95e144 (in Russian). are situated in region with 50-meter depth that is also character- Nam KB, Lee KG, Hwang JW, Yoo JC. 2014. Variation in breeding burrows of Streaked ized with the presence of circular currents and joints of multidi- Shearwaters breeding in Sasu Island, and predation rates by Norway . Ocean Polar Res 36:49e57 (In Korean). rectional currents. The most biologically important feature of such Sailing direction of the north-western coast of the Sea of Japan from Tumannaya river areas is the high concentration of zooplankton. to Belkin cape. St. Peterburg. 308 p. (in Russian). Shuntov VP. 1965. Seasonal aspects in marine birds distribution in the open waters of the Sea of Japan. Zoologicheskii Zhurnal 44:411e422 (in Russian). Conflicts of interest Shuntov VP. 1998. Birds of the far eastern seas of Russia. Vladivostok: TINRO-tzentr 1. 423 p. (in Russian). The authors declare that there is no conflicts of interest. Yamamoto T, Takahashi A, Oka N, et al. 2011. Foraging areas of Streaked Shearwaters in relation to seasonal changes in the marine environment of Northwestern Pacific: inter-colony and sexual differences. Marine Ecology Progress Series 424: References 191e204. Yoshida N. 1962. Breeding ecology of the Streaked Shearwater at Kamurijima I. e Dolganova TN, Nadtochii VV. 2015. Composition, seasonal and annual dynamics of Maizuru in Kioto 17:79 108. zooplankton in the Peter the Great Bay (the Sea of Japan). Izvestiya TINRO 181: Yoshida N. 1981. Ki ni noboru umidori: Kityo ohmizunagidori (Climbing the trees: 169e190 (in Russian). Streaked Shearwaters with interesting behavior). Tokyo: Chobun Sya Co. Ltd.. in Amirkhanov AM, et al., editors. 2001. The Red book of the Russian Federation (Ani- Japanese. mals)//Under supervision of V.I. Danilov-Danilyan. Moscow: Astrel. 860 p. (in Russian).